Africa's Circumcision

NEWS FEATURE

Africa’s circumcision CHALLENGE To combat the spread of HIV, health officials plan to circumcise 20 million men in Africa, but some have concerns about the aftermath.

BY CATHERINE DE LANGE

arvin is 22 years old, single and — like many men of his age in clinical trials will not bear out to the same Circumcision packets — thinking about girlfriends. But for the next six weeks, he degree when scaled up to tackle a messy epi- at a clinic in Zambia. will have to give his love life a rest. On this sunny morning demic that is spread as much through behaviour in the Zambian capital, Lusaka, Marvin is waiting to get as biology. In particular, they say that men are getting mixed messages Mcircumcised. Along with three of his friends, he sits tensely on a bench about the benefits of circumcision. Another concern is the effect on outside the operating theatre, a room usually used for abortions. Are women, who gain no direct protection from the circumcision campaign, they nervous? Marvin cracks a wide smile. “A little,” he says. and may even face greater risk. Critics say the programmes could increase In Lusaka, young men like Marvin have grown up with daily remind- the risk of HIV infection in some populations by encouraging people to ers of the risks that can accompany sexual relationships. For years, bill- engage in risky sexual behaviours, such as forgoing condoms. boards and adverts painted on walls have espoused the importance of “It’s only been shown to decrease to some degree transmission from safe sex and testing for HIV, which currently infects more than one in the female to the male, and yet we are acting as if it’s the only thing to do,” five Lusaka residents. But more recently, a new message has been pop- says Philip Thuma, a doctor who runs the Malaria Institute at Macha ping up in public spaces and the media: a call for men to get circumcised in southern Zambia. “Our job as scientists is to step back and be a bit to reduce their chances of contracting the virus. Marvin’s friends told sceptical. Should we really be putting this much emphasis on something him about the procedure. “A lot of them have been circumcised so I at the expense of other things that are just as important?” thought of doing the same thing,” he says, adding that it may increase his odds with women. “I hear that the first thing they ask you is ‘have POINT OF ENTRY you been circumcised?’” he says. But, ultimately, he hopes the surgery The idea that circumcision might reduce the risk of HIV infection is will help him “just to stay healthy”. often traced back to Valiere Alcena, a physician now at the Albert Ein- Scenes like this have become familiar across much of southern and stein College of Medicine in New York City, who noted in 1986 that eastern Africa. Since 2007, 14 nations have taken part in a massive public- the men of Haiti and Central Africa are usually uncircumcised and as health campaign aimed at circumcising millions of men in an attempt a result often develop lesions on the foreskin that serve as a potential to drastically reduce the spread of HIV (see ‘Making the cut’). About entry point for AIDS1. The idea was cemented when a landmark study2 3 million men in the region have been circumcised since the start of the in 1989 showed that of some 400 Kenyan men who visited a group of campaign, and the initiative was made a high priority in late 2011 by prostitutes with high rates of HIV, those who were not circumcised had the World Health Organization (WHO), the Joint United Nations Pro- more than eight times the risk of becoming infected than those who gramme on HIV/AIDS (UNAIDS) and the US President’s Emergency were. Michel Garenne, a demographer at the Pasteur Institute in Paris, Plan for AIDS Relief (PEPFAR) — which are funding part of the pro- remembers being at a meeting when the paper was first presented, and gramme. The rest is being provided by the Bill & Melinda Gates Founda- it seemed to make sense. “I was working in Senegal, where there was tion, the World Bank and other global health organizations. The targets very little AIDS and a lot of circumcision, so I became quite convinced are ambitious: 80% of men of reproductive age in these countries need to that something was going on,” he says. be circumcised by 2015. That means more than 20 million circumcisions. But others disagreed, arguing that some populations did not fit If these efforts succeed, the payoff could be considerable. Reaching the this pattern and that the correlation could be 80% goal could cut the number of new HIV infections in the target coun- NATURE.COM explained by other factors relating to the preva- tries by as much as half, says Bertran Auvert, a public-health specialist at For an online lence of circumcision, such as religious practice. the University of Versailles Saint-Quentin-en-Yvelines in Paris. “The goal slideshow and audio Garenne himself became sceptical. In 1994, he is to have a huge impact on the overall HIV epidemic in Africa.” content, see: was working in South Africa, where he found a But some scientists worry that the benefits reported for circumcision go.nature.com/dtgxyn huge HIV epidemic even though many men were

circumcised. “I changed my mind and became convinced that circumcision will never help in controlling HIV/AIDS,” he says. Those who did believe in the protective effect of circumcision called for a systematic analysis to settle the matter. Three randomized clinical trials were carried out in southern Africa between 2002 and 2007. One study3, led by Auvert, offered medical circumcision to men in a region of DE LANGE CATHERINE South Africa and compared them with a non-circumcised group. After 21 months, there were 20 cases of HIV in the circumcised group and 49 among the uncircumcised men, equating to a 60% reduction in HIV risk. Two other trials, in Kenya4 and Uganda5, produced similar results. “It’s extraordinary in any public-health measure that you get such consistency of results,” says Robert Bailey, an epidemiologist at the University of Illinois at Chicago, who led the Kenyan study. The WHO also found the consistency compelling and declared the results “an important landmark in the history of HIV prevention”. In 2007, the WHO, UNAIDS and PEPFAR recommended implementing voluntary medical male circumcision (VMMC) in 14 high-risk African countries. ‘A MAN WHO CARES’ Zambia, with its high prevalence of HIV, low circumcision rates and mixed attitudes towards circumcision, is a microcosm of the broader campaign. During the past five years, it has seen the progressive roll- out of catchy, pro-circumcision slogans on posters, television and radio campaigns. Health-service providers have also developed outreach programmes to spread the message. At the clinic where Marvin is waiting, visitors are greeted by an adver- tisement for its services: a silhouette of a man standing proudly with his hands hooked inside his belt and, above it, a slogan reading: “Male Cir- cumcision, a man who cares”. Clinics that perform the procedure hope the belt-hook stance will become an unspoken symbol, a way for men to implicitly communicate their circumcised status, which is increasingly viewed as an attractive attribute. If the campaigns can convince enough men to take part, the programme could significantly reduce HIV-transmission rates, accord- ing to a number of modelling studies. These project that circumcising 80% of men aged 15–49 years old in targeted countries by 2015 would decrease the incidence of HIV by 30–50% over 10 years, amounting to some 3.4 million fewer new infections. Carrying out these 20.3 million circumcisions by 2015, plus an additional 8.4 million over the following 10 years, would cost about US$2 billion, but would potentially save $16.5 billion by 2025 owing to avoided treatment and care costs6. There may be other benefits too. Before men undergo voluntary medical circumcision, many get an HIV test, which means more cases of HIV will be picked up, and thus more men will be referred for treatment. “I think circumcision is going to have a very significant impact because it’s being delivered as a package,” Bailey says. A big part of that package is a one-on-one counselling session run by people such as Jonathan Kabanda, a counsellor for the Society for Family Health in Livingstone, about five hours’ drive south of Lusaka. It is his job to make sure that men who come in for circumcision understand the benefits and the risks, not only for themselves but also for their partners. On a Saturday morning, Kabanda sits down and arranges his materials, among them three large wooden phalluses — one equipped with a retractable fabric foreskin — and some condoms. He pulls out a small flip chart that details different matters relating to circumcision — starting with how the foreskin can increase the transmission of HIV and leading on to the benefits and limitations of circumcision. Those who support the campaigns, including the WHO, PEPFAR and the authors of the clinical trials, stress the importance of making sure that patients understand that circumcision provides limited protection and that men should continue to use condoms. But critics ask whether the message is getting through. There is certainly room for confusion. Although Kabanda’s presentation is thorough, one page of the flip chart, titled ‘MC does not offer 100% protection’ shows a picture of a man chasing two women down the street while throwing his condoms away.

MAKING THE CUT Since health trials in Africa demonstrated that circumcision lowers rates of HIV transmission, donor nations and charities have poured more than US$100 million into circumcision campaigns in 14 African nations. But they have a long way to go to reach the goal of 20 million circumcisions by 2015.

50 1.8 Public Zimbabwe Namibia Philanthropic 1.6 Zambia Mozambique Total global investment Uganda Malawi 40 1.4 Tanzania Lesotho Swaziland Kenya South Africa Ethiopia Foundations have 1.2 Rwanda Botswana 30 ramped up support for circumcision campaigns. 1.0

0.8 20 0.6

0.4

Annual investments (US$ millions) 10

Number of male circumcisions (millions) 0.2

0 0 2006 2007 2008 2009 2010 2011 2012 2009 2010 2011 2012

Other benefits are overstated: “You are preventing your partner from Layer, a health-communications researchers at the Johns Hopkins Uni- cervical cancer,” Kabanda says, when, in fact, the reduction in risk is far versity in Baltimore, Maryland, explored that possibility by interviewing from complete. 33 women following a circumcision campaign in the city of Iringa in Outside the clinic in Lusaka, it is clear Marvin has also received mixed Tanzania. She found an overwhelming preference for circumcised men8; messages from his counselling session. “We were told there was a sixty- women believed them to be cleaner and better educated. Some women SOURCE: UNAIDS something per cent of being … I don’t know if it’s from HIV or some also assumed — incorrectly — that the reduced risk of contracting HIV sexually transmitted disease,” he says. “And the 45%, I don’t know what applied to women, too. As one woman who was interviewed for the it is; I didn’t get much about that. I think I’ll try to ask later.” study put it: “Circumcised men who are HIV-positive can have sex with Many men may face similar confusion. As part of the procedure, par- women and the women will not get the infection easily.” ticipants get only one counselling session on the matter of circumcision Much of the research on risk compensation relies on self-reported and one with their HIV test. By contrast, the men in the clinical trials had behaviours and often involves qualitative studies. But Layer’s interviews sessions before and after circumcision, and every six months during the showed consistent misunderstandings about circumcision, a finding 21-month follow-up period. Some public-health advocates argue that the borne out by studies in other countries that suggest women are less protocols used in the trials should be replicated closely in the campaigns, likely to require circumcised men to use a condom. “There is evidence otherwise they will not be as effective. “When technologies like male cir- in South Africa, Kenya and Tanzania that shows that generally women cumcision are demonstrated effective, everybody forgets about the rest are overstating the benefits of circumcision and believe the risk to be of the protocol and just looks at the medical procedure,” says Seth Kalich- lower than it actually is,” she says. man, a clinical psychologist at the University of Connecticut in Storrs who Other studies, however, suggest that circumcision does not lead to more studies behavioural responses to HIV-prevention campaigns. “We need to risky behaviour by men and women. Earlier this year, Auvert published think about the standard of care within which a procedure is implemented findings from a survey9 in the same region as his original trial in 2005. He if we’re going to hope to get the effects that we saw in the trial.” found that despite a high uptake of circumcision, there was no reported However, in a campaign that aims to reach millions of men, it would difference in sexual behaviour — for instance in condom use or number be hard to get participants to return for regular counselling. And some of partners — between circumcised and uncircumcised men, and the esti- researchers, such as Auvert, dismiss the importance of counselling, argu- mated HIV incidence rate was around 60% lower among the circumcised ing that it has little impact on behaviour. “If counselling was enough to group. Similarly, when Bailey and his colleagues did a follow-up study in change sexual behaviour to reduce the risk of acquiring HIV, we would Kenya, they found no increase in risk associated with the circumcision. have stopped the HIV epidemic in Africa a long time ago,” he says. Researchers are at odds over the implications. “Any public-health measure will have the potential for risk compensation, but there is no RISK ASSESSMENT evidence at all that risk compensation is taking place and indeed there The question of behaviour has become a crucial one in the debate over is some evidence that the opposite is occurring,” Bailey says. circumcision. A chief concern is that men and women who believe Kalichman disagrees. He believes that men are getting mixed mes- that they are less likely to acquire HIV will engage in more risky sexual sages, and that it doesn’t make sense that they would agree to circumci- behaviour. This means that circumcision “could have the opposite effect sion if they were going to consistently use condoms, which offer a much in the long run”, Garenne says. “People might be more likely to get HIV higher level of protection. “Why bother with the procedure if you have than if they were not circumcised at all.” to continue to use condoms?” he asks. “The whole point is, ‘if I have the Studies of this phenomenon — known as risk compensation — are procedure I don’t need to’.” just starting to shed light on how circumcision alters behaviour, and so The take-home message on risk compensation, he says, is that “we far the findings are mixed. In one survey7 conducted in Kenya directly don’t know the extent of it and we also don’t know the impact of it”. It is before the circumcision scale-up took place, Bailey and his colleagues possible, he adds, that the overall effect is minor because the 60% risk- reported that one-fifth of men and women they interviewed said that reduction offered by circumcision is already so substantial. condom use is less necessary and that HIV is a less serious threat because Nonetheless, Layer says it is important to make sure women are also male circumcision is available. targeted by clear messages about the limitations of circumcision. “If we These misconceptions could put women at particular risk. Erika do a little bit more to try to engage women I think we could reduce the

Billboard adverts and family-planning programmes are helping to spread the message about the benefits of male circumcision.

immediate and the long-term risk for both women and men,” she says. or financial incentives for referrals. More money is also being invested, Circumcision advocates say that in the long run, a general reduction but this has put significant pressure on local service providers to operate in HIV prevalence in the population will ultimately benefit women, on more men. The Bill & Melinda Gates Foundation, based in Seattle, even if some women are placed at greater risk in the short term. “I am Washington, has implemented a pay-for-performance model in Zambia, absolutely convinced that some women will become HIV positive for instance, in which organizations are reimbursed on the basis of their because of the circumcision of their partners,” says Auvert. However, he ability to reach a target number of circumcisions. “I think you have to be adds that he will publish some preliminary results soon showing that the concerned about the impact on quality of such an incentives approach,” impact on women is extremely small. “We are not concerned,” he says. says one person familiar with the programme who wished to remain The issue of balancing individual risks against widespread benefits anonymous. He wonders whether it could cause circumcision providers also comes up in studies looking at how many men have sex during the to cut costs for other essential services, such as counselling. In a state- healing period after circumcision, when open wounds and unhealed ment to Nature, Sema Sgaier, a senior programme officer with the Gates stitches increase the risk of transmission. In the counselling session, Foundation, wrote “to ensure that VMMC delivery does not affect estab-

PHILIMON BULAWAYO/REUTERS; CATHERINE DE LANGE CATHERINE PHILIMON BULAWAYO/REUTERS; men are told to abstain from sex for six weeks lished standards of care, it is always delivered as or, if they can’t wait, to use a condom. How- one component of a comprehensive package of ever, a study10 by Paul Hewett of the Population “THERE IS NO services”. These include HIV counselling and Council in Lusaka and his colleagues found that testing as well as screening and treatment for around one-quarter of men said they resumed EVIDENCE AT other sexually transmitted diseases. sex prematurely; of those, 82% engaged in at Everybody from donors to doctors in the least one act of unprotected sex, and a number ALL THAT RISK clinic agrees that the circumcision effort must had unprotected intercourse with two or more be part of a broader strategy to strangle Africa’s partners. When the team modelled the effect COMPENSATION IS HIV epidemic. And although the 20-million of this on HIV transmission, it estimated that if goal remains distant, the campaigns could still 61,000 men were circumcised in one year, early TAKING PLACE.” bring major benefits, says Bailey. “Even if you resumption of sex would result in a total of 69 don’t reach the 80% target that’s not to say you’re extra HIV infections. But the overall net effect was protective, with 230 not going to have a large impact on the number of new infections,” he fewer HIV infections in one year, predominantly among men. says. “Every circumcision still has a preventive effect.” For people living in the epicentre of the HIV epidemic, that protective TARGET DRIVEN effect — however limited — is an attractive offering. Marvin, for one, Both critics and advocates of the circumcision campaigns agree that it is confident in his decision. “I think, for me,” he says, “it’s going to be a will be a struggle to reach the 20-million mark by 2015, given that so far good thing.” ■ SEE EDITORIAL P.165 countries have only reached 15% of that overall goal. At health clinics across Zambia, much of the conversation is about targets, says Layer. Catherine de Lange is an editor with Nature in London. She travelled “This seems to be the trend — do whatever it takes to get men in and to Zambia on a fellowship from the International Reporting Project at out that door,” she says. So circumcision providers are coming up with Johns Hopkins University in Baltimore, Maryland. innovative ways to recruit more men. The US embassy in Zambia has 1. Alcena, V. NY State J. Med. 86, 446 (1986). launched a new effort to work with chiefs of traditionally non-circumcis- 2. Cameron, D. W. et al. Lancet 334, 403–407 (1989). ing tribes in the hope that they will “convince their own people that even 3. Auvert, B. et al. PLoS Med. 2, e298 (2005). though this isn’t a part of their historic tradition this is the right choice”, 4. Bailey, R. C. et al. Lancet 369, 643–656 (2007). 5. Gray, R. H. et al. Lancet 369, 657–666 (2007). says Mark Storella, the US ambassador to Zambia. And mobile clinics 6. Njeuhmeli, E. et al. PLoS Med. 8, e1001132 (2011). travel to hard-to-reach areas to recruit men. “There’s a lot of pressure 7. Westercamp, M., Agot, K. E., Ndinya-Achola, J. & Bailey, R. C. AIDS Care 24, right now in this country because of PEPFAR and others,” says Thuma. 157–166 (2012). 8. Layer, E. H. et al. PLoS ONE 8, e74391 (2013). The recruitment drive is happening across the region. In Kenya, some 9. Auvert, B. et al. PLoS Med. 10, e1001509 (2013). service providers are even offering ‘moonlight circumcisions’ at night, 10. Hewett, P. C. et al. AIDS 26, 749–756 (2012).